Phase shifts and the stability of macroalgal communities on Caribbean coral reefs

Caribbean coral reefs are widely thought to exhibit two alternate stable states with one being dominated by coral and the other by macroalgae. However, the observation of linear empirical relationships among grazing, algal cover and coral recruitment has led the existence of alternate stable states to be questioned; are reefs simply exhibiting a continuous phase shift in response to grazing or are the alternate states robust to certain changes in grazing? Here, a model of a Caribbean forereef is used to reconcile the existence of two stable community states with common empirical observations. Coral-depauperate and coral-dominated reef states are predicted to be stable on equilibrial time scales of decades to centuries and their emergence depends on the presence or absence of a bottleneck in coral recruitment, which is determined by threshold levels of grazing intensity and other process variables. Under certain physical and biological conditions, corals can be persistently depleted even while increases in grazing reduce macroalgal cover and enhance coral recruitment; only once levels of recruitment becomes sufficient to overwhelm the population bottleneck will the coral-dominated state begin to emerge. Therefore, modest increases in grazing will not necessarily allow coral populations to recover, whereas large increases, such as those associated with recovery of the urchin Diadema antillarum, are likely to exceed threshold levels of grazing intensity and set a trajectory of coral recovery. The postulated existence of alternate stable states is consistent with field observations of linear relationships between grazing, algal cover and coral recruitment when coral cover is low and algal exclusion when coral cover is high. The term ‘macroalgal dominated’ is potentially misleading because the coral-depauperate state can be associated with various levels of macroalgal cover. The term ‘coral depauperate’ is preferable to ‘macroalgal dominated’ when describing alternate states of Caribbean reefs.     

Competition between herbivourous fishes and urchins on Caribbean reefs

Summary When the common sea urchin Diadema antillarum was removed from a 50 m strip of reef in St. Thomas, US Virgin Islands, cover of upright algae and the grazing rates and densities of herbivorous parrotfish and surgeonfish increased significantly within 11–16 weeks when compared to immediately adjacent control areas. Sixteen months after removal, Diadema had recovered to 70% of original density, abundance of upright algae no longer differed between removal and control areas, and the abundance and grazing activity of herbivorous fish in the removal was approaching equivalence with control areas. On a patch reef in St. Croix that had been cleared of Diadema 10–11 years earlier (Ogden et al. 1973b), urchins had recovered to only 50–60% of original density. This reef still showed significantly higher rates of grazing by fish and a significantly greater density of parrotfish and surgeonfish than a nearby control reef where Diadema densities had not been altered. These results indicate that high Diadema densities (7–12/m² for this study) may suppress the densities of herbivorous fish on Caribbean reefs.     

Testing relationships between macroalgal cover and Secchi depth in the Baltic Sea

The present study tests whether relationships between macroalgal cover and water quality, recently developed for Danish coastal waters, are more universal and also applies at the other extreme of the Baltic Sea in Finnish coastal waters. We found that algal cover increases as a function of Secchi depth according to the same logarithmic function in Danish and Finnish coastal waters. Algal cover at a given depth (here modelled for 4 m) increases with increasing Secchi depth and approaches a maximum at the high Secchi depths found in the clearest areas of the Danish coastal waters. For a given Secchi depth the combined Danish/Finnish algal model thus predicts a similar cover of the algal community at a given water depth at both extremes of the Baltic Sea which represent quite different algal habitats. These results suggest that light limitation, and thus shading effects of eutrophication may cause similar reductions of macroalgal cover across ecosystems.     

Hysteresis in coral reefs under macroalgal toxicity and overfishing

Macroalgae and corals compete for the available space in coral reef ecosystems.While herbivorous reef fish play a beneficial role in decreasing the growth of macroalgae, macroalgal toxicity and overfishing of herbivores leads to proliferation of macroalgae. The abundance of macroalgae changes the community structure towards a macroalgae-dominated reef ecosystem. We investigate coral-macroalgal phase shifts by means of a continuous time model in a food chain. Conditions for local asymptotic stability of steady states are derived. It is observed that in the presence of macroalgal toxicity and overfishing, the system exhibits hysteresis through saddle-node bifurcation and transcritical bifurcation. We examine the effects of time lags in the liberation of toxins by macroalgae and the recovery of algal turf in response to grazing of herbivores on macroalgae by performing equilibrium and stability analyses of delay-differential forms of the ODE model. Computer simulations have been carried out to illustrate the different analytical results.

Electronic Supplementary Material

The online version of this article (doi:10.1007/s10867-014-9371-y) contains supplementary material, which is available to authorized users.     

Competitive interactions between corals and Trididemnum solidum on Mexican Caribbean reefs

The ascidian Trididemnum solidum competes for space on Caribbean reefs and is capable of overgrowing live scleractinian corals. From 2006 to 2009, we monitored over 30,000 coral colonies and quantified competitive interactions with this ascidian at four reef sites along the Mexican Caribbean. The total number of competitive interactions increased in time, but the mean percentage of coral colonies involved in interactions remained lower than 1% in all reefs. Bottom cover by T. solidum was also low (mean < 0.5%) in all reef sites in all sampling years. We conclude that during the temporal scope of our study, the overall potential effect of T. solidum on the dynamics of Mexican Caribbean coral populations was minimal.     

Relationships between macroalgal biomass and microbiological quality of water in a phytotreatment pond

The microbiological quality of wastewater in phytotreatment ponds with foliose macroalgae can be influenced by biofilm formation on thallus surface. This hypothesis was tested with an in situ experiment which was carried out in a pond with Ulva spp. receiving wastewater from a land based fish farm at Piombino (Italy). The total bacterial load (TBL) was determined in the inflowing and outflowing waters and a multifactorial design was employed to investigate the effect of different macroalgal biomass. Microbiological analysis revealed a high TBL in the water column (18.4 ± 7.4 × 10⁸ cells ml⁻¹). TBL of inlet water was significantly correlated with quantity and quality of particulate organic matter (POM) of inflowing water, whereas no correlation was found between TBL and POM in the outlet water. A significant decrease in the POM concentration was detected within macroalgal ponds, due to the mechanical action of thalli which favoured POM sedimentation. Nevertheless, great TBLs were found in the outlet water. These findings suggest that TBL probably depended upon macroalgae. Indeed high bacterial density was found on macroalgal thallus surface (~10⁸ cells cm²). Furthermore, high plate counts of faecal bacteria (faecal enterococci) were determined on thallus surface (~ 40 CFU cm²) and outlet water (11 886 ± 3984 CFU 100 ml⁻¹) supporting the evidence that macroalgae negatively affect the microbiological quality of treated water. Bacterial activities in terms of exoenzymatic rates and secondary production were two folds higher in the water within macroalgal beds, than in the open water. These preliminary results suggest that high macroalgal biomass represents a ‚hot spot’ of bacterial density and activity that may affect microbiological quality of the treated water. Bacterial control of inlet water and management of macroalgal biomass through periodic removal are essential for a more efficient treatment of wastewater in phytotreatment ponds.     

Diversity and extinction in the Cenozoic history of Caribbean reefs

Occurrences of reef corals are examined at Caribbean fossil localities to determine how biodiversity has changed within the region over the past 50 million years. Analyses of 294 species (66 genera) at 58 fossil localities show that Caribbean generic diversity rose to 44 between 50–22 Ma, ranged from 32–39 between 22–2 Ma, and dropped to 25 afterwards. Regional species diversity was high at 40–36 Ma, 28–22 Ma, and 5–2 Ma. Origination rates were elevated throughout each high diversity interval, but extinction was concentrated near the end of each interval. Regional highs of origination and extinction, therefore, differed in timing and duration, causing the observed regional diversity increases during the three remarkably long intervals of turnover. Highs of generic origination decreased in magnitude as immigration from the Mediterranean ceased, but speciation highs increased in association with emergence of the Central American isthmus. Peaks of extinction coincided with regional changes in climate and oceanic circulation. Maximum species diversities within assemblages increased to 40–60 between 50–36 Ma, and have remained relatively constant ever since. Assemblage compositions differed among localities having similar ages and environments, suggesting that the timing and pattern of turnover varied across the region. Stable diversities but variable compositions within assemblages suggest that dispersal and recruitment influenced the pattern of faunal change during turnover. Accepted: 22 August 1999     

A connection between colony biomass and death in Caribbean reef-building corals

Increased sea-surface temperatures linked to warming climate threaten coral reef ecosystems globally. To better understand how corals and their endosymbiotic dinoflagellates (Symbiodinium spp.) respond to environmental change, tissue biomass and Symbiodinium density of seven coral species were measured on various reefs approximately every four months for up to thirteen years in the Upper Florida Keys, United States (1994-2007), eleven years in the Exuma Cays, Bahamas (1995-2006), and four years in Puerto Morelos, Mexico (2003-2007). For six out of seven coral species, tissue biomass correlated with Symbiodinium density. Within a particular coral species, tissue biomasses and Symbiodinium densities varied regionally according to the following trends: Mexico≥Florida Keys≥Bahamas. Average tissue biomasses and symbiont cell densities were generally higher in shallow habitats (1-4 m) compared to deeper-dwelling conspecifics (12-15 m). Most colonies that were sampled displayed seasonal fluctuations in biomass and endosymbiont density related to annual temperature variations. During the bleaching episodes of 1998 and 2005, five out of seven species that were exposed to unusually high temperatures exhibited significant decreases in symbiotic algae that, in certain cases, preceded further decreases in tissue biomass. Following bleaching, Montastraea spp. colonies with low relative biomass levels died, whereas colonies with higher biomass levels survived. Bleaching- or disease-associated mortality was also observed in Acropora cervicornis colonies; compared to A. palmata, all A. cervicornis colonies experienced low biomass values. Such patterns suggest that Montastraea spp. and possibly other coral species with relatively low biomass experience increased susceptibility to death following bleaching or other stressors than do conspecifics with higher tissue biomass levels.     

The effects of macroalgal cover on the spatial distribution of macrobenthic invertebrates: the effect of macroalgal morphology

The growth of green macro-algae in response to nutrient inputs is a common phenomenon in marine estuaries and sheltered bays. While the ecological effects of the growth of the most commonly occurring macroalgal taxa (Enteromorpha, Chaetomorpha, Ulva, Cladophora) have been well studied, the effects of a morphologically very different species, Vaucheria subsimplex, have not been investigated. This study investigated the ecological effects of the establishment of V. subsimplex on a relatively exposed intertidal sandflat, Drum Sands, Firth of Forth, Scotland. Because of the spatially heterogeneous development of the weed, the short term (4 weeks) and long term (20 weeks) effects of the weed could be studied using a survey approach in which the weed-affected and weed-free plots were interspersed. After 4 weeks, V. subsimplex significantly increased the mean number of individuals and diversity of the macrofauna, eight of the ten most abundant species showed significant increases in abundance compared to weed-free areas. After 20 weeks, mean number of species and individuals were significantly higher under weed patches, while species diversity was reduced due to the numerical dominance of Pygospio elegans (Claparède). The weed, therefore, had an enriching effect on the macrofaunal communities on Drum Sands. The increased numbers of P. elegans, the numerical dominant infaunal species on Drum Sands, resulted mainly from enhanced larval recruitment to weed-affected areas. The effects of V. subsimplex on sediment characteristics were similar to those reported for other macroalgal taxa, i.e., increased water, organic and silt/clay contents, medium particle size and sorting coefficients, and reduced redox potentials. The results from this study are compared to those for other, morphologically different macroalgal species, with particular reference to an Enteromorpha-implanted experiment on the same sandflat. Since the general effect of such macroalgal taxa on macrofaunal communities is a detrimental one, the present study supports the contention that macroalgal morphology is an important feature in algal–faunal interactions.     

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

The effect of fishing on hysteresis in Caribbean coral reefs

Coral resilience is important for withstanding ecological disturbances as well as anthropogenic changes to the environment. However, the last several decades have demonstrated a decline in resilience that has often resulted in phase shifts to a degraded coral-depleted state with high levels of algal abundance. A major defining issue in current research is to identify when and how it is possible to reverse these phase shifts allowing for the ecosystem to escape coral depletion and maintain coral-based ecosystem services. We extend an analytic model to focus on the effects of over-harvesting of herbivorous reef fish in the Caribbean by explicitly including grazer dynamics which introduces feedbacks between habitat and grazer abundance posing constraints on management options excluded in previous studies. This allows us to develop ecosystem-based management recommendations for two distinct scenarios of coral reef recovery: The first follows significant habitat damage in response to a large disturbance and the second maintains reef structure but has suffered from events such as coral bleaching. We identify critical fishing effort levels to allow for coral recovery and demonstrate that regions exhibiting severe damage to reef structure have little resilience implying that fishing reductions should be coupled with other restoration methods. Regions that are coral-depleted but maintain reef structure allow for recovery given sufficiently small levels of fishing mortality. However, we demonstrate the difference in recovery time in response to varying levels of control efforts on fishing.     

Drivers of region-wide declines in architectural complexity on Caribbean reefs

Severe declines in the cover of live hard coral on reefs have been reported worldwide, and in the Caribbean region, the architectural complexity of coral reefs has also declined markedly. While the drivers of coral cover loss are relatively well understood, little is known about the drivers of regional-scale declines in architectural complexity. We have used a dataset of 49 time series reporting reef architectural complexity to explore the effect of hurricanes, coral bleaching and fishing on Caribbean-wide annual rates of change in reef complexity. Hurricane impacts greatly influence reef complexity, with the most rapid rates of decline in complexity occurring at sites impacted during their survey period, and with lower rates of loss occurring at unimpacted sites. Reef architectural complexity did not change significantly following mass bleaching events (in a time frame of <5 years) or positive thermal anomalies. Although the rates of change in architectural complexity were similar in and out of marine protected areas (MPAs), significant declines in complexity were observed inside but not outside of MPAs, possibly because reductions in fishing can lead to increased bioerosion by herbivores within MPAs. Our findings suggest that major drivers of coral mortality, such as coral bleaching, do not influence reef architectural complexity in the short term (<5 years). Instead, direct physical impacts and reef bioerosion appear to be important drivers of the widespread loss of architecturally complex reefs in the Caribbean.     

Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs

Coral-algal symbiosis has been a subject of great attention during the last two decades in response to global coral reef decline. However, the occurrence and dispersion of free-living dinoflagellates belonging to the genus Symbiodinium are less documented. Here ecological and molecular evidence is presented demonstrating the existence of demersal free-living Symbiodinium populations in Caribbean reefs and the possible role of the stoplight parrotfish (Sparisoma viride) as Symbiodinium spp. dispersers. Communities of free-living Symbiodinium were found within macroalgal beds consisting of Halimeda spp., Lobophora variegata, Amphiroa spp., Caulerpa spp. and Dictyota spp. Viable Symbiodinium spp. cells were isolated and cultured from macroalgal beds and S. viride feces. Further identification of Symbiodinium spp. type was determined by length variation in the Internal Transcribed Spacer 2 (ITS2, nuclear rDNA) and length variation in domain V of the chloroplast large subunit ribosomal DNA (cp23S-rDNA). Determination of free-living Symbiodinium and mechanisms of dispersal is important in understanding the life cycle of Symbiodinium spp.     

White-band disease and the changing face of Caribbean coral reefs

In recent decades, the cover of fleshy macroalgae has increased and coral cover has decreased on most Caribbean reefs. Coral mortality precipitated this transition, and the accumulation of macroalgal biomass has been enhanced by decreased herbivory and increased nutrient input. Populations of Acropora palmata (elkhorn coral) and A. cervicornis (staghorn coral), two of the most important framework-building species, have died throughout the Caribbean, substantially reducing coral cover and providing substratum for algal growth. Hurricanes have devastated local populations of Acropora spp. over the past 20–25 years, but white-band disease, a putative bacterial syndrome specific to the genus Acropora, has been a more significant source of mortality over large areas of the Caribbean region.Paleontological data suggest that the regional Acropora kill is without precedent in the late Holocene. In Belize, A. cervicornis was the primary ecological and geological constituent of reefs in the central shelf lagoon until the mid-1980s. After constructing reef framework for thousands of years, A. cervicornis was virtually eliminated from the area over a ten-year period. Evidence from other parts of the Caribbean supports the hypothesis of continuous Holocene accumulation and recent mass mortality of Acropora spp. Prospects are poor for the rapid recovery of A. cervicornis, because its reproductive strategy emphasizes asexual fragmentation at the expense of dispersive sexual reproduction. A. palmata also relies on fragmentation, but this species has a higher rate of sexual recruitment than A. cervicornis. If the Acropora spp. do not recover, macroalgae will continue to dominate Caribbean reefs, accompanied by increased abundances of brooding corals, particularly Agaricia spp. and Porites spp. The outbreak of white-band disease has been coincident with increased human activity, and the possibility of a causal connection should be further investigated.     

A clear human footprint in the coral reefs of the Caribbean

The recent degradation of coral reefs worldwide is increasingly well documented, yet the underlying causes remain debated. In this study, we used a large-scale database on the status of coral reef communities in the Caribbean and analysed it in combination with a comprehensive set of socioeconomic and environmental databases to decouple confounding factors and identify the drivers of change in coral reef communities. Our results indicated that human activities related to agricultural land use, coastal development, overfishing and climate change had created independent and overwhelming responses in fishes, corals and macroalgae. While the effective implementation of marine protected areas (MPAs) increased the biomass of fish populations, coral reef builders and macroalgae followed patterns of change independent of MPAs. However, we also found significant ecological links among all these groups of organisms suggesting that the long-term stability of coral reefs as a whole requires a holistic and regional approach to the control of human-related stressors in addition to the improvement and establishment of new MPAs.     

Species density and associations in Caribbean reef corals

The density of scleractinian corals on portions of two reefs in the Grenadine Islands, W. I. has been investigated by direct observation by SCUBA divers. Grid, transect, and random quadrat methods were compared with total samples to determine the precision and accuracy of these techniques. Transect methods were generally satisfactory provided at least 15% of a 400 m² total grid area was included in the sample. The data strongly indicated clumped distributions of all species, although numerical analysis does not indicate the distinct zones reported by other workers. Species associations based on Jaccard's coefficient and cluster analysis showed possible similarities in physical requirements, although few strong associations were found. Data based on 4 m² quadrats generally provided a more reliable estimate of species associations than did data based on 1 m² quadrats. It is suggested that surveys of these reef types may be better based on a number of parallel transects rather than a single transect, and that well-defined zones are more likely to be the exception than the rule.     

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

Benthic-pelagic coupling on coral reefs: Feeding and growth of Caribbean sponges

Benthic-pelagic coupling and the role of bottom-up versus top-down processes are recognized as having a major impact on the community structure of intertidal and shallow subtidal marine communities. Bottom-up processes, however, are still viewed as principally affecting the outcome of top-down processes. Sponges on coral reefs are important members of the benthic community and provide a crucial coupling between water-column productivity and the benthos. Other than scleractinian corals, sponges dominate many of these habitats where water column productivity is composed of mostly autotrophic and heterotrophic picoplankton that sponges actively filter. While predation upon sponges by invertebrates, fish, and turtles occurs, the sponges Callyspongia vaginalis, Agelas conifera, and Aplysina fistularis from Florida, Belize, and the Bahamas, respectively, exhibit a consistent and significant pattern of greater biomass, rates of growth, and feeding, as does their food supply, with increasing depth. Sponges consume 65-93% of the available particulate food supply and, at all sites, sponges increase in size and growth rate as depth increases, suggesting that food supply and, therefore, bottom-up processes significantly influence the distribution and abundance of sponges in these habitats.     

Current patterns of macroalgal diversity and biomass in northern hemisphere rocky shores

Latitudinal gradients in species abundance and diversity have been postulated for nearshore taxa but few analyses have been done over sufficiently broad geographic scales incorporating various nearshore depth strata to empirically test these gradients. Typically, gradients are based on literature reviews and species lists and have focused on alpha diversity across the entire nearshore zone. No studies have used a standardized protocol in the field to examine species density among sites across a large spatial scale while also focusing on particular depth strata. The present research used field collected samples in the northern hemisphere to explore the relationships between macroalgal species density and biomass along intertidal heights and subtidal depths and latitude. Results indicated no overall correlations between either estimates of species density or biomass with latitude, although the highest numbers of both were found at mid-latitudes. However, when strata were examined separately, significant positive correlations were found for both species numbers and biomass at particular strata, namely the intertidal ones. While the data presented in this paper have some limitations, we show that latitudinal macroalgal trends in species density and biomass do exist for some strata in the northern hemisphere with more taxa and biomass at higher latitudes.